Phosphorylation of the compartmentalized PKA substrate TAF15 regulates RNA-protein interactions

Cell Mol Life Sci. 2024 Apr 3;81(1):162. doi: 10.1007/s00018-024-05204-4.

Abstract

Spatiotemporal-controlled second messengers alter molecular interactions of central signaling nodes for ensuring physiological signal transmission. One prototypical second messenger molecule which modulates kinase signal transmission is the cyclic-adenosine monophosphate (cAMP). The main proteinogenic cellular effectors of cAMP are compartmentalized protein kinase A (PKA) complexes. Their cell-type specific compositions precisely coordinate substrate phosphorylation and proper signal propagation which is indispensable for numerous cell-type specific functions. Here we present evidence that TAF15, which is implicated in the etiology of amyotrophic lateral sclerosis, represents a novel nuclear PKA substrate. In cross-linking and immunoprecipitation experiments (iCLIP) we showed that TAF15 phosphorylation alters the binding to target transcripts related to mRNA maturation, splicing and protein-binding related functions. TAF15 appears to be one of multiple PKA substrates that undergo RNA-binding dynamics upon phosphorylation. We observed that the activation of the cAMP-PKA signaling axis caused a change in the composition of a collection of RNA species that interact with TAF15. This observation appears to be a broader principle in the regulation of molecular interactions, as we identified a significant enrichment of RNA-binding proteins within endogenous PKA complexes. We assume that phosphorylation of RNA-binding domains adds another layer of regulation to binary protein-RNAs interactions with consequences to RNA features including binding specificities, localization, abundance and composition.

Keywords: ALS; Affinity purification; Colon cancer; FET-protein; Interaction network; Molecular interactions; Neurodegeneration; Post-translational modification; Proteomics.

MeSH terms

  • Amyotrophic Lateral Sclerosis*
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Humans
  • Phosphorylation
  • RNA
  • TATA-Binding Protein Associated Factors*

Substances

  • Cyclic AMP-Dependent Protein Kinases
  • Cyclic AMP
  • RNA
  • TAF15 protein, human
  • TATA-Binding Protein Associated Factors